Scientometric review of research on Neglected Tropical Diseases: a 31-year perspective from the Journal of the Brazilian Society of Tropical Medicine

ABSTRACT Background: To analyze the temporal evolution of research on Neglected Tropical Diseases (NTDs) published by the Journal of the Brazilian Society of Tropical Medicine (JBSTM). Methods: We performed an analysis of the scientific production in JBSTM on NTDs using an advanced search, which included authors’ descriptors, title, and abstract, and by combining specific terms for each NTDs from 1991 to 2021. Data related to authors, countries of origin, institutions, and descriptors, were evaluated and analyzed over time. Bibliographic networks were constructed using VOSviewer 1.6.16. Results: The JBSTM published 4,268 scientific papers during this period. Of these 1,849 (43.3%) were related to NTDs. The number of publications on NTDs increased by approximately 2.4-fold, from 352 (total 724) during 1991-2000 to 841 (total 2,128) during 2011-2021, despite the proportional reduction (48.6% versus 39.5%). The most common singular NTDs subject of publications included Chagas disease (31.4%; 581/1,849), leishmaniasis (25.5%, 411/1,849), dengue (9.4%, 174/1,849), schistosomiasis (9.0%; 166/1,849), and leprosy (6.5%, 120/1,849), with authorship mostly from Brazil’s South and Southeast regions. Conclusions: Despite the proportional reduction in publications, JBSTM remains an important vehicle for disseminating research on NTDs during this period. There is a need to strengthen the research and subsequent publications on specific NTDs. Institutions working and publishing on NTDs in the country were concentrated in the South and Southeast regions, requiring additional investments in institutions in other regions of the country.


INTRODUCTION
Neglected tropical diseases (NTDs) cause high morbidity and mortality and are strongly associated with poverty and inequality. They affect populations with limited access to health services; have varied biological and transmission characteristics; and can be caused by fungi, viruses, bacteria, protozoa, arthropods, snakes, and helminths 1,2 . NTDs are present in more than 149 countries and have an annual financial impact on the world economy of billions of dollars 3 . In addition, approximately two billion people are at risk of developing one or more NTDs 3,4 .
Worldwide, five NTDs are the most commonly studied: dengue, soil-transmitted helminthiases, leishmaniasis, Chagas disease, and schistosomiasis. Among these diseases, dengue is the fastestgrowing in terms of the number of publications associated with people living in resource-poor communities in urban centers in developing countries, in addition to epidemic areas in Southeast Asia and Brazil 8 .
As in other countries, the classification of NTDs in Brazil has changed over time as diseases are included and removed. In 2005, the Ministry of Health of Brazil research and development program considered the addition of six diseases to the list of epidemic/endemic NTDs: dengue, malaria, tuberculosis, Chagas disease, leishmaniasis, and leprosy. In 2008, schistosomiasis was added. The report "Health Brazil 2017: an analysis of the health situation and the challenges for the achievement of the Sustainable Development Goals" under Chapter 5 ("Neglected diseases in Brazil: vulnerability and challenges") considered Chagas disease, schistosomiasis mansoni, leprosy, lymphatic filariasis, tegumentary leishmaniasis, visceral leishmaniasis, onchocerciasis, human rabies, and trachoma to be NTDs 7,9 . The WHO list includes NTDs present in Brazil, Latin America, and other African and Asian continents 3 .
Each of these diseases has specific characteristics in various Brazilian epidemiological contexts; some are in the different stages of control 10 . Considering the current pandemic caused by the new coronavirus (SARS-CoV-2) and its potential impact, the future epidemiological scenario for NTDs is uncertain owing to the weakening of control actions, as well as limited access to health care, diagnosis, and treatment for affected people. There are delays in manufacturing, shipment, transport, and delivery of drugs; reassignment of personnel; and diversion of financial resources. Currently, areas negatively impacted by COVID-19 primarily include community interventions; early diagnosis; access to treatment and care in the health services network; monitoring and evaluation activities; reallocation of financial resources to other "priority" actions; and relocation of teams for surveillance, care, and control of NTDs to support actions to combat the virus 11 .
The official journal of the Brazilian Society of Tropical Medicine (BSTM), the Journal of the Brazilian Society of Tropical Medicine (JBSTM), presents primarily in the context of Brazilian and Latin American spaces and follows a multidisciplinary perspective. The papers can be assessed openly, and submissions are published 100% free of charge. The journal publishes original research on NTDs, preventive medicine, public health, infectious diseases, and related subjects. JBSTM was founded in 1962 as a channel for scientific dissemination. The first issue was released in 1967, with five articles on schistosomiasis 12 . Here, we present a scientometric review of NTDs in the JBSTM from 1991 to 2021.

Type of study
The current study is a scientometric review of NTDs published by JBSTM and indexed in the Scopus® database accessed through the Federated Academic Community of the Coordination for the Improvement of Higher Education Personnel (in portuguese: Comunidade Acadêmica Federada da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior [CAFe-CAPES]) (https://www.scopus.com/home.uri). All types of scientific productions on NTDs published by JBSTM were included, independent of the country of origin and publication: original articles, editorials, review articles, short communications, case reports, technical reports, images of infectious diseases, letters, supplements, and obituaries.

Source and organization of data
Database searches (deadline: July 27, 2022) were completed using specific criteria and the advanced search function by applying the author's descriptors, title, and abstract, combining specific terms for each NTD ( Table 1). The NTDs were selected based on a group of 20 diseases defined by WHO 2 . All publications from January 1991 to December 2021 were considered and screened. Data on all authors, country of origin, institutions, and health descriptors were extracted and analyzed, and the number and proportion of scientific production over time was evaluated. All authors (with their country of origin and affiliation) included in the scientific publications were considered.
An author's country of origin and affiliated institutions were considered to be the first information reported by the author, as manuscripts were counted as a unit of analysis. The relationship analysis was carried out using the scientometric visualization software VOSviewer 1.6.16 (https://www.vosviewer.com/) based on the structuring of the bibliographic networks and the specificities of the references associated with each record, in addition to the author's descriptor data and the arrangement of the most frequent terms in the publications.
Data were analyzed for the complete period and stratified into four periods (1991-2000, 2001-2010, 2011-2021, and 1991-2021); the change from 1991 to 2021 was then compared. To demonstrate the evolution of scientific production over time, graphs were constructed; data depicted were on the number and proportion of publications on NTDs in JBSTM and the NTDs with the highest proportion of scientific publications. Tables were organized by decades to present independent NTDs, types of scientific products, authors, descriptors, affiliations, and countries.

Analysis of the bibliometric profile
Representative images of the relationships (maps) between authors, countries, institutions, and descriptors (nodes), the strength between these relationships (thickness of the arcs), and the number of their total contributions (node size), are presented. The "thesaurus" (VOSviewer tool) was applied to consolidate terms. The parameters considered were a maximum limit of "25" and a minimum of "2" for items of scientometric identification of each unit of analysis: 1) co-authorship by author; 2) co-authorship by countries; 3) co-authorship by organizations; and 4) co-occurrence of author keywords, linked to the bibliographic production relationship network and aggregated over the entire study period. For some parameters, we calculated the 95% confidence intervals (CI).

Ethical aspects
The present study was based on JBSTM publications available on the 100% open access journal's website (https://www.scielo.br/j/rsbmt/) free of charge. Thus, according to national guidelines, submission to a research ethics committee is not necessary. This study followed the ethical recommendations of the National Health Council (Resolution No. 466 of 2012).

General profile
During  Table 2). There was a reduction in the relative number of publications made from 2017 onwards, with <40% occurring from 2018 to 2021. Some diseases also showed a reduction in the absolute number and percentage of publications ( Figure 1A and Figure 1B).
Brazil appeared most frequently among authorships in the JBSTM publication, followed by other Latin American countries (Argentina and Mexico) during 1991-2000. There was a change in this profile during the 2001-2010 and 2011-2020 periods, with a greater number originating from the United States of America, Spain, and Belgium, among others ( Table 3).  Table 3).
Chagas disease stood out for the period, with an average by-year proportion of 33.9% (95% CI, 29.9-37.9) for publications related to NTDs (in terms of number and percentage). Among the five NTDs with the highest number of publications in the JBSTM, only publications on dengue showed an increasing pattern over the analyzed period ( Figure 1A and Figure 1B).
For co-authorship of author relationships, from 1991-2021, 1,306 authors with more than two documents were identified and organized into 33 clusters, and the eight most productive clusters showed more than 37 correlated authors. The most prominent authors with articulated connections are "Prata A." and "Lambertucci J.R.". (Figure 2A).
The co-authorship and organization relationship presented a pattern among the institutions for the 1991-2021 period, with 167 presenting more than two publications, and was organized into 16 clusters. The leading institution for scientific production was the "Fundação Oswaldo Cruz (Fiocruz) -Rio de Janeiro", followed by the "Universidade de São Paulo". Notable volumes were also completed by the "Universidade Federal de Minas Gerais", "Universidade de Brasília", "Centro de Pesquisa René Rachou (Fiocruz) -Minas Gerais", "Universidade Federal do Triângulo Mineiro", and "Universidade Federal do Ceará" (Figure 2B). The analysis of co-authorship across countries showed a predominance of Brazilian connections to other countries. We identified 34 countries in which authors presented two or more publications. The strongest cooperation links were observed between Brazil and the United States, Argentina, and the United Kingdom ( Figure 2C).
An analysis of the co-occurrence of author keywords for the 1991-2021 period identified 467 descriptors, with two or more citations, and was organized into 36 clusters. The most prominent cluster is "leishmaniasis," followed by "Chagas disease". Other secondary clusters are also noteworthy, such as "schistosomiasis," "leprosy," "Trypanosoma cruzi", and "epidemiology" (Figure 2D). During this period, most of the published articles were in the English language (62.5%; 2669/4268).

DISCUSSION
We found that the vast majority of papers were published by Brazilian authors, and whether a disease was endemic or not to Brazil did not play a role in the published studies. This is not a surprise, as among the diseases defined as NTDs by the WHO, some are not considered endemic or do not occur in Brazil. The JBSTM, through its traditions, national reach, and interdisciplinary openness, tends to aggregate Brazilian researchers and expand on collaborations with other countries; this is due to a need to prioritize the journal's theme, progressive increase in international visibility, and its impact factor, to aid in the achievement of of the Millennium Development Goals (MDGs) formulated in the years 2000 13 . There were additional scientific productions in the JBSTM linked to institutions in the South and Southeast of Brazil, likely due to the distribution of teaching and research institutions in Tropical Medicine, and the differential funding available from governments and funding agencies. This difference may be due to tradition, better environment, and infrastructure. Given the endemic contexts of Brazil and Latin America, it is important to recognize the outstanding number of publications on Chagas disease, leishmaniasis, schistosomiasis, dengue, and leprosy; these account for most of the publications on NTDs in the JBSTM in human, parasitological, and entomological research. There are other factors contributing to the greater number of Brazilian authors published in the JBSTM, such as the inclusion of articles written in Portuguese until 2012 and the tendency of the BSTM to publish their work in this journal.
Since JBSTM publishes articles on research conducted in Brazil and Latin America 12 , diseases with more publications reflects those which are a priority for Brazil and are present in the list of compulsory notifications 14 . NTDs with the highest percentage of scientific production in the JBSTM (with an increase or decrease in the absolute number and percentage over time) are endemic in Brazil, with a considerable number of cases recorded every year, or even in epidemic years, such as dengue 7,9,10 .
In recent decades, there have been constant changes to the world demography, which may influence the increases in infectious diseases (especially NTDs): high population growth, acceleration of urbanization, increased life expectancy, decreased fertility rates, and population aging. These changes have influenced the unplanned growth of cities associated with poverty, unemployment, inadequate housing, agglomerations, increased vector-borne diseases, increased vehicle traffic, environmental degradation, and pollution. Such variations also represent changes in the behavior of different agents that cause infectious diseases 15 .
National and international agendas highlighting NTDs from the year 2000 13 did not increase the number and/or percentage of publications in the JBSTM, either in general or in specific productions, as demonstrated in other studies 8,16,17 . This change may also be related to evolutions in the pattern of research, with the search for journals with higher ratings primarily according to the impact factor occurring more frequently, as it was a requirement of research funding agencies. NTDs are included in research calls for proposals from funding agencies such as CNPq In the Brazilian context, the "Qualis Periódicos" of CAPES has also regulated the standards of publications related to postgraduate programs in the country, which has brought significant impacts, such as driving leading researchers and postgraduate students to seek journals with better ranking 18 .
JBSTM has many publications on endemic NTDs in Brazil 9 . This pattern differs from that found in research from other Latin American countries, where dengue usually has the highest average proportion of studies, followed by leishmaniasis, Chagas disease, and schistosomiasis 19 . The fact that JBSTM represents the Brazilian context from a greater perspective means that some diseases stand out as containing a greater number of publications, particularly because they are public health problems and are highlighted in government agendas 7,9 . Articles and reviews were among the most common publication types accepted by JBSTM, similar to those found in other studies using a general approach from various journals 19,20 . The two most commonly accepted formats are based on the traditional formats of NTDs articles published in scientific journals 7 .
The scientific production of NTDs in JBSTM is highlighted among authors when considering references for their work with specific diseases, such as schistosomiasis 21 , Chagas disease 22,23 , and leishmaniasis 24 . The most cited authors, besides being references in their areas of expertise, also contributed to the consolidation of public health policies, such as chronic Chagas disease, which became a compulsory notification in May 2020 22,23,25 .
The most commonly mentioned descriptors for the retrieval of scientific productions on NTDs from JBSTM revealed a strategic pattern of publications in the journal, a fact not observed in other scientific journals that publish on diseases with more general endemic characteristics in Latin America, Asia, and other continents 19,26,27 . The descriptors express the general aspects recommended by government agencies, with priority for recurrent diseases in the Brazilian scenario, and consequently, the area of expertise of the JBSTM authors 7,9,22 . Climate change scenarios may contribute to the emergence and/or re-emergence of some NTDs, especially those transmitted by vectors or intermediate hosts; consequently, research published in JBSTM could contribute to surveillance and monitoring 28 . Some institutions have a higher proportion of publications in JBSTM, mainly those from the states of Rio de Janeiro, Minas Gerais, and São Paulo, with an increased number from the northeast region: Centro de Pesquisas Aggeu Magalhães (Fiocruz Pernambuco), Universidade Federal de Pernambuco, and Universidade Federal do Ceará; and in the North region: Fundação de Medicina Tropical Doutor Heitor Vieira Dourado (Amazonas). This pattern is not significantly different from the international pattern of other journals that publish on NTDs and institutions, where these institutions are also hegemonic 16,29 . This difference occurs mainly in the funding that these research institutions receive from the development agencies 30 . However, research could be directed towards the presentation of strategies for the control and elimination of NTDs present in the national scenario and Latin America, which will be even more relevant in the pandemic context and for the future post-pandemic, with the risk of even more limited resources for the resumption of public health programs in the coming years 31 .
Due to the Brazilian context, the majority of JBSTM publications are concentrated from Brazil; however, affiliations in institutions from other countries in Latin America, North America, Europe, and Asia have publications and connections with Brazilian authors. This is similar to the results presented in a study that evaluated publications in NTDs in Latin America and the Caribbean 19 . The coauthorship connections between scientific production in the United States of America increased after 2000, with the prioritization of NTDs in international agendas 2,13 . Other studies have also shown Brazil's connection to other countries 16,32 .
This study presents with limitations, such as the use of a single database (Scopus®). In addition, Scopus® groups the publications from "Images in Infectious Diseases" or "Case Reports" in the articles. the search based on the selection of scientific production from terms in the titles, abstracts, and keywords for greater sensitivity; the affiliation between countries of the authors, facts that may not translate the reality due to the quality of the filling out that, in some cases, it is not possible to recognize the institution; the absence of analysis of the citation profile of the manuscripts approaching different diseases analyzed. Despite such limitations, the findings of the current study are justified and contribute to the evaluation of the current scenario of scientific production of NTDs in one of the traditional journals which is also most relevant to Brazilian Tropical Medicine.

CONCLUSION
JBSTM remains an important vehicle for disseminating research on NTDs during this period despite the proportional reduction seen in recent years. The disparity between the institutions that work and publish NTDs in the country is evident. There is a need to strengthen the research and subsequent publications on NTDs. Institutions working and publishing on NTDs in the country were